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provided by Springer - Publisher Connector Aquat Ecol (2011) 45:75–87 DOI 10.1007/s10452-010-9333-9

Abiotic factors affecting the development of Ulva sp. (; ) in freshwater ecosystems

Beata Messyasz • Andrzej Rybak

Received: 26 January 2010 / Accepted: 7 July 2010 / Published online: 20 July 2010 Ó The Author(s) 2010. This article is published with open access at Springerlink.com

Abstract The influence of physicochemical factors with stable and deeper water, the surface area of the on the development of Ulva species with distromatic mats was larger. Both phosphate and nitrite concen- tubular morphology was studied in three streams trations were positively correlated with an increase in located in Poznan, . The study evaluated key the number of thalli in the mats and the thalli length. environmental factors that may influence the coloni- sation and growth of Ulva populations in freshwater Keywords Ulva Chlorophyta Macroalgae mats systems. In total, nine environmental parameters were PCA Ecology Nutrients included: temperature, water depth, pH, oxygen (O2), ? - ammonium (NH4 ), nitrate (NO3 ), phosphate 3- (PO4 ), sodium chloride (NaCl) and total iron Introduction (Fe). Morphometric features of thalli (length and width, percentage of furcated and young thalli) and The cosmopolitan genus Ulva (Fish and Fish 1989; surface area of free-floating mats formed by the Fletcher 1996; Callow et al. 1997;Ba¨ck et al. 2000; freshwater populations of Ulva were compared at all Gabrielson et al. 2000; Graham and Wilcox 2000; sites. Principal components analysis indicated the Blomster et al. 2002; Hayden et al. 2003; Leskinen most important factors influencing Ulva development et al. 2004) is mostly found in marine and brackish were sodium chloride concentrations and water waters (Kirchhoff and Pflugmacher 2002; Lee 1999; depth. Two other key chemical factors affecting the Romano et al. 2003) and estuaries (Ba¨ck et al. 2000; freshwater form of Ulva were phosphate and nitrite McAvoy and Klug 2005). It can also be present in concentrations. High concentrations of sodium chlo- freshwaters, often in ecosystems located far inland on ride inhibited the development of Ulva, leading to a continents and islands that are not in contact with salt lower number of thalli in the Ulva mats. At the sites waters. During the 20th century, such freshwater Ulva populations have been recorded in eight coun- tries, including Great Britain (Whitton and Dalpra 1968), the United States (Taft 1964; Reinke 1981), Handling editor: Piet Spaak. the Czech Republic (Maresˇ 2009), (Ichihara et al. 2009), Pakistan (Leghari et al. 2000), New B. Messyasz (&) A. Rybak Zealand (Williams 1993) and Poland (Messyasz and Department of Hydrobiology, Institute of Environmental Rybak 2009). Biology, Faculty of Biology, Adam Mickiewicz University, Umultowska Str. 89, 61-614 Poznan, Poland Thirteen species of Ulva have been reported from e-mail: [email protected] the Polish Baltic coastline (Plin´ski et al. 1982; Plin´ski 123 76 Aquat Ecol (2011) 45:75–87 and Florczyk 1984). Typically, marine Ulva species using examples from three streams in Poland. An have also been observed in several freshwater systems additional concern was to evaluate the impact on in Poland (Go¨ppert and Cohn 1850; Kozłowski 1890; Ulva species in freshwater ecosystems, associated Raciborski 1910; Wysocka 1952; Piotrowska 1961; with anthropogenic sodium chloride pollution and Plin´ski 1971; Sitkowska 1999; Messyasz and Rybak nutrient (N and P) enrichment. 2009). Between 1849 and 2007, five species and one subspecies of Ulva were observed at 58 inland sites in Poland (Messyasz and Rybak 2009). These occurred Materials and methods as either single or large concentrations of thalli in various freshwater ecosystems, mostly lakes, but also Study area in small rivers, streams and ponds. Other sites included peat pits, clay pits and stream basins. The The study sites containing Ulva were located in most common species at these inland Polish sites three *0.5-m deep steams in the south-eastern area included Ulva intestinalis (34 sites), U. flexuosa of Poznan´, Poland (Fig. 1). Two sites containing Ulva (10 sites), U. prolifera (5 sites) and U. compressa were in the Michało´wka stream (52°2002000N, (4 sites). Also, the rarest Ulva species in Polish 17°0204400E and 52°2002100N, 17°0204500E) and one in freshwaters, U. paradoxa, has been observed at only the Dworski Ro´w stream (52°2102800N, 17°0203000E). 2 sites, while the subspecies U. flexuosa subsp. The sites in Michało´wka and Dworski Ro´w were pilifera has been seen at 3 locations. located 541 m from each other. Another location Young Ulva have a thallus that remains either containing these macroalgae was in the S´wia˛tnica attached to a substrate or they can develop unat- stream (52°2103900N, 17°0204200E), which is 4.5 km tached, as drifting individuals or as aggregations of from the other two sites. All sites containing Ulva were free-floating mats (Bliding 1963, 1968; Starmach in the vicinity of a motorway. The Michało´wka sites 1972). Freshwater forms of Ulva appear only as (hereinafter ‘‘M1’’and ‘‘M2’’)were 34 m and 19 m from monostromatic tubular thalli (e.g. Ulva intestinalis the motorway, respectively. The third site in Dworski and Ulva compressa). So far, Ulva with distromatic Ro´w (hereinafter ‘‘DR’’) was 425 m from the motorway, frondose thalli has not been reported in freshwater and the fourth one in S´wia˛tnica (hereinafter ‘‘S’’) ecosystems (Messyasz and Rybak 2009). Mature was located 246 m from the motorway. plants of freshwater Ulva can have one of the two types of thalli surface architecture. One has an intestinally undulating thallus with a smooth surface, Chemical analysis and the other is curly bubbled with a strongly corrugated and often highly furcated thallus (Marczek The physicochemical parameters of waters from the 1954). It has been frequently observed that a few four sites containing Ulva were analysed when the Ulva species form freely floating thallus mats macroalgae thalli were present, i.e., from August (Fletcher 1996; Callow et al. 1997; Blomster et al. until October, 2007. Water temperature, pH and 2002). Their appearance in a marine littoral zone has oxygen levels were measured using Elmetron been related to the nutrient enrichment of littoral CX-401 and CPC-501 protocols with this analysis, waters (Wallentinus 1979; Sfriso and Marconimi repeated weekly. Additionally, changes in water 1997; Raffaelli et al. 1989; Martins et al. 2001; depth, thickness of bottom sediments and shading Zbikowski_ et al. 2005). of the sites by vascular plants (immersed and floating) This paper’s objective is to provide additional were monitored. Water samples (500 mL) were information to previous ecological studies of fresh- collected for chemical analyses and preserved with water Ulva populations in Poland. Detailed ecolog- 0.5 ml of chloroform. These samples were then ical studies of parameters that influence the stored in refrigerators at 4°C, with chemical analyses occurrence of Ulva species in freshwaters need to performed using standard methods for a Hach DR be investigated. Therefore, the goal of this work was 2010 spectrophotometer. Concentrations were deter- to determine the influence of the colonisation and mined for the following variables: ammonium, growth of Ulva populations in freshwater ecosystems nitrate, phosphate, sodium chloride and iron. 123 Aquat Ecol (2011) 45:75–87 77

Fig. 1 Location of the sampling sites of freshwater Ulva populations in the Wielkopolska region (Central , Poland, Poznan City). 1 motorway, 2 streams, 3 water channels, 4 roads, 5 railway, 6 forests, 7 built-up areas, 8 meadows

Both the percentage of water surface area covered and morphometric features of thalli defined using by Ulva thalli and the density of Ulva thalli per m-2 Pearson’s linear correlation coefficient including r2 of surface water were evaluated in the field. The ratio. A PCA (principal components analysis) method lengths and widths of thalli taken from each site were was used to compare the diversity of physicochemical also measured. The morphometrical measurements environmental parameters and then to determine were repeated ex situ on material preserved with relationships to the Ulva populations. formalin (4% concentration). Macroalgae mats were analysed to determine the number of furcated thalli and the presence of young and mature plants. Results

Statistical analysis Physicochemical profiles of the study sites

STATISTICA 7.0 and CANOCO 6.2. software were During the study period (July–October 2007), water used for the statistical analysis of the collected data. temperature and pH values were similar for all sites. The correlation between physicochemical parameters The highest water temperature was at S because of 123 78 Aquat Ecol (2011) 45:75–87

Table 1 Average values of physicochemical factors of water for the examined sites

Parameter Units M1 M2 DR S

Temperature (8C) 14.77 (2.56) 15.09 (2.68) 14.75 (2.73) 15.72 (2.48) pH – 8.16 (0.67) 8.11 (0.64) 8.04 (0.52) 7.97 (0.70) Depth of water (cm) 50.12 (19.36) 44.00 (22.76) 48.68 (9.60) 16.25 (3.07) -1 O2 (mg L ) 2.26 (1.29) 2.12 (1.47) 0.52 (0.20) 4.00 (0.78) ? -1 N-NH4 (mg L ) 1.34 (1.19) 1.44 (1.18) 0.90 (0.82) 0.31 (0.58) - -1 N-NO3 (mg L ) 0.64 (0.36) 0.70 (0.37) 0.40 (0.35) 0.05 (0.02) 3- -1 P-PO4 (mg L ) 0.71 (0.15) 0.74 (0.19) 0.19 (0.11) 0.02 (0.01) NaCl (mg L-1) 544.97 (38.33) 549.25 (26.77) 651.35 (81.30) 697.51 (78.87) Total Fe (mg L-1) 0.29 (0.24) 0.31 (0.18) 1.18 (0.62) 0.04 (0.03)

Data are means (SD); n = 30; M1, M2, DR and S—sites the shallow water level of the watercourse (average Similar values in the results of these sites may be temperature of 15.72°C at an average depth of associated with their close proximity to each other in 16.25 cm). Measurements of pH for all four sites Michało´wka stream. were approximately 8.0 (Table 1). The lowest oxygen concentrations were at DR (0.52 mg L-1), and at the other three sites, where the Phenology of Ulva waters could mix as they flowed, with a more open surface area, the oxygen levels were higher. The From August 5 until October 2, 2007, characteristics highest oxygen concentrations (4.0 mg L-1) were at of Ulva thalli were examined and recorded from the S where there was a strong current flow in the stream. three streams. During this period, the number of thalli

M1 and M2 had higher concentrations of phos- at a given site, and consequently the mats formed by phates in comparison with the other water courses. this species, underwent changes that were monitored. -1 The lowest values of P-PO4 were at S (0.01 mg L ). In July and in early August at each of the Ulva The opposite situation occurred for sodium chloride monitoring locations, filamentous algae of the genera content in the other streams, where the lowest Cladophora sp. and Oedogonium sp. were the concentrations were observed for both M sites dominant flora in the surface water. However, the -1 (M1—544.97 and M2—549.25 mg L ). A higher abundance of these species declined in mid-August salt level was measured at DR (651.35 mg L-1), and when the concentration of Ulva thalli significantly the highest was found at S (697.51 mg L-1). increased. During this period, the Ulva mats covered Higher levels of ammonium nitrogen were also at 60–90% of the stream’s width, and Ulva became the -1 -1 M1—1.34 mg L , M2—1.44 mg L and DR—0.90 dominant species of the surface water layer. Also, the mg L-1 in comparison with S (0.06 mg L-1). A filamentous algae were observed at the bottom of similar situation was observed for nitrite content in the M1 and DR stations. At the end of August, after the waters from the M1, M2 and DR, with the nitrite the developmental optimum of Ulva, it was evident level much higher (M1—0.64; M2—0.70; DR— that there was an intensive growth of vascular plants 0.40 mg L-1), while in the S site the concentration that were freely floating on the water’s surface at all was only 0.05 mg L-1 (Table 1). sites containing macroalgae. Lemna gibba, Lemna Waters from DR had the highest concentrations of minor and occasionally Spirodela polyrrhiza began to total iron, at 1.18 mg L-1 compared to the other sites gradually displace Ulva from the water’s surface in -1 (M1—0.29; M2—0.31; S—0.01 mg L ). each of the streams. After August 20, a complex of Both M1 and M2 were very similar in regard these pleustophytes species covered the entire water to most physicochemical factors, i.e., water surface at M1, M2 and DR. Domination by duckweed depth, concentration of oxygen, phosphate, nitrate, and Spirodela was not observed in S´wia˛tnica due to sodium chloride, ammonium nitrogen and iron. the rapid water flow in this stream. 123 Aquat Ecol (2011) 45:75–87 79

Morphometric characteristics of Ulva recorded at DR and S of *6m-2 and *2m-2, respectively. The longest and widest thalli occurred at

Ulva thalli growing in the streams formed floating M1 (average length—14.15 cm, average width— mats (macroalgae scum). However, each mat for a 0.82 cm) and M2 (average length—12.42 cm, aver- given site had a characteristic number of thalli, age width—0.89 cm). The thalli of Ulva from DR structure and surface density in the water column. and S were shorter and narrower than those from The largest Ulva mats exceeded *2m2 and appeared Michało´wka (Table 2). Furcated and non-furcated at M1 and M2 (Table 2). thalli surface architecture was recorded at all sites. Both M1 and M2 contained abundant Ulva thalli, At M1 and S, the percentage of the furcated thalli which always formed one larger and denser mat and a density mat was over 40%, and at the other sites it few smaller ones with a loose structure, located near was[20%. In every mat from a given stream, mature stream banks. At the end of August, the mat’s surface thalli constituted more than 60% of the mat. The 2 area was the largest at M1 measuring about 4 m .In percentage of mature thalli in mats was highest in the same period at M2, the macroalgae mat was ca. S´wia˛tnica, where it exceeded 90%. 2m2. At DR, the mats were smaller, their surface area rarely exceeded 1 m2 and their structure was not Effect of water chemistry on Ulva development dense. The smallest mats were recorded at S, with the surface covering only 0.10–0.30 m2. In this study, the most important factors affecting The thalli density in the mats was different for morphological development of Ulva were depth and every site. For the M1 and M2, thalli densities were sodium chloride concentration (Fig. 2). These param- *52 m-2 and *44 m-2, respectively. In S´wia˛tnica eters explained 83 and 88%, respectively, of the and Dworski Ro´w, the lowest thalli densities were variability in the data obtained from the studied sites.

Table 2 Average values of morphometric thalli features and Ulva mats

Parameters Units M1 M2 DR S

Surface of the mats (m2) 1.84 (1.36) 1.17 (0.63) 0.51 (0.17) 0.15 (0.08) Density of thalli in m-2 of the mats (m-2) 52.88 (25.68) 44.71 (9.88) 6.33 (1.75) 2.83 (1.17) Average length of the thallus (cm) 14.15 (3.83) 12.42 (2.58) 6.63 (2.16) 7.14 (1.86) Average width of the thallus (cm) 0.82 (0.47) 0.89 (0.48) 5.53 (0.14) 0.61 (0.25) The percentage of the branched thallus in m-2 of the mats (%) 41.67 (23.37) 20.71 (32.46) 26.67 (27.87) 41.65 (35.87) The percentage of the unbranched thallus in m-2 of the mats (%) 58.33 (23.32) 79.28 (32.46) 73 (27.87) 85.33 (35.87) The percentage of the young thallus in m-2 of the mats (%) 37.78 (37.76) 15.71 (18.13) 25.83 (34.70) 5.83 (3.76) The percentage of the mature thallus in m-2 of the mats (%) 62.22 (37.66) 84.28 (18.13) 74.17 (34.70) 94.17 (3.76)

Data are means, (SD), n = 30, M1, M2, DR and S—sites

Fig. 2 The PCA diagram for individual physicochemical factors of water from four freshwater Ulva sites 123 80 Aquat Ecol (2011) 45:75–87

Fig. 3 Results of PCA grouping at all sites on the basis of water physicochemical factors (M1, M2, DR and S—sites)

Fig. 4 Correlation between the density of Ulva thalli in The parameters that correlated with the first PCA axis macroalgal mats and different phosphate concentration in accounted for 64.5% of the variability, whereas those water habitat. Pearson coefficient of correlation: 0.70; P \ 0.01; n = 30 that correlated with the second axis explained 23.5% of the variability (Fig. 2). The PCA measurements allowed classification of Parameters such as water depth and concentrations of the physicochemical data into three different groups sodium chloride, nitrate and phosphate considerably representing the three studied streams. The analysis affected development of the macroalgae thalli. The confirmed that both M1 and M2 have very similar analysis showed that a concentration of phosphate physiochemical parameters, while DR and S differ was positively correlated with the density of thalli in from each other and from M (Fig. 3). macroalgal mats (r = 0.70; P \ 0.01; r2 = 0.48; On the basis of a Pearson linear correlation test Fig. 4) and thalli length (r = 0.59; P \ 0.01; (significance level of P \ 0.01) and a sample size of r2 = 0.35). n = 30, four of the nine studied physicochemical Another important parameter that influenced the parameters were significantly correlated with mor- development of Ulva was sodium chloride. Sodium phometrical features of the Ulva thalli (Table 3). chloride was negatively correlated with the thalli

Table 3 Coefficients of linear Pearson’s correlation (r) and the coefficient of determination (r2) values among morphometric features of Ulva thalli with physicochemical factors

Feature/parameter Depth NaCl P-PO4 N-NO3 (cm) (mg L-1) (mg L-1) (mg L-1)

Density of thalli in m-2 of the mats 0.54** -0.68** 0.70** 0.56** [0.29] [0.47] [0.48] [0.31] Surface of the macroalgae mats 0.48** -0.55** 0.52** – [0.23] [0.30] [0.27] – Average length of the thallus 0.38* -0.64** 0.59** – [0.14] [0.40] [0.35] – The percentage of the young thallus in m-2 of the mats 0.54** -0.40* – – [0.29] [0.16] – – The percentage of the mature thallus in m-2 of the mats -0.54** 0.40* – – [0.29] [0.16] – – * P \ 0,05; ** P \ 0,01; [r2]; n = 30 123 Aquat Ecol (2011) 45:75–87 81

Discussion

Marine and freshwater Ulva species

The bloom development of Ulva species is uncommon in inland waters. As a marine species Ulva typically has a cosmopolitan range and appear only occasion- ally in inland freshwater ecosystems. They occur in ecosystems with elevated concentrations of chlorides and biogenic nutrients. In Poland, Ulva species have been observed in inland salt waters (Raciborski 1910; Namysłowski 1927), salt marshes (Piotrowska 1961; Wilkon´-Michalska 1963) and peat pits (Plin´ski 1971, 1973a, 1973b). In those ecosystems, high concentra- tions of chlorides are natural, and the conditions are Fig. 5 Correlation between the density of Ulva thalli in similar to those of littoral seawaters. These conditions macroalgal mats and different sodium chloride concentration in have contributed to the permanent habitation of Ulva water habitat. Pearson coefficient of correlation: -0.68; intestinalis in the mineral spring area of Ciechocinek P \ 0.01; n = 30 since as early as the 19th century (Go¨ppert and Cohn 1850; Kozłowski 1890) and later in other regions of density (per m2) of mats (r =-0.68; P \ 0.01; Poland where salt waters are present (Torka 1910; r2 = 0.47; Fig. 5) and the thalli length of the Liebetanz 1925). However, Ulva species were also macroalgae (r =-0.64; P \ 0.01; r2 = 0.40). A observed in freshwater systems, which are not natu- high water concentration of sodium chloride inhibited rally supplied with mineral waters possessing high thalli elongation and development and led to a sodium chloride concentrations. A dozen or so of decrease in the number of thalli in mats, especially these macroalgae sites have been found in lakes in young plants (r =-0.40; P \ 0.05; r2 = 0.16). (Torka 1910; Plin´ski 1973a; Kowalski 1975; Increasing concentrations of sodium chloride that Da˛mbska 1976; Messyasz 2009), fishponds (Marczek inhibited thalli development ultimately result in a 1954; Piotrowska 1961; Kowalski 1975; Sitkowska reduction of the mat’s surface development. Increas- 1999), rivers (Wysocka 1952; Kowalski 1975; Endler ing water depth for all Ulva sites was positively et al. 2006), canals and streams (Liebetanz 1925; correlated with the thalli density of mats and the Kowalski 1975; Messyasz and Rybak 2009). percentage of young plants per mat (r = 0.54; Studies investigating species of Ulva, typically P \ 0.01; r2 = 0.29). Increasing water depth also have been observed in freshwater ecosystems where positively correlated with the mat’s surface area low concentrations of chlorides were recorded but (r = 0.48; P \ 0.01; r2 = 0.23) and thalli length have provided little information concerning the (r = 0.38; P \ 0.05; r2 = 0.14). The water depth phylogeny of these macroalgae. The genetic analyses was also negatively correlated with the percentage of of Ulva species based on sequencing nuclear-encoded older algae per mat (r =-0.54; P \ 0.01; 18S rDNA have identified relationships among Ulva r2 = 0.29). Therefore, it is highly probable that deep populations in different ecosystems. Examinations of water restricts the number of mature individuals in two populations of Ulva in freshwater ecosystems mats. Also, nitrate concentration, was positively (river and stream) on Ryukyu island (Japan) resulted correlated with thalli density of the mats (r = 0.54; in identifying a new species (Ulva limnetica Ichihara P \ 0.01; r2 = 0.31). Therefore, a higher concentra- and Shimada, sp. nov; Ichihara et. al. 2009). Subse- tion of nitrate resulted in an increasing number of quently, Maresˇ (2009) phylogenetically tested 20 thalli forming the macroalgae mat. The analysis populations of Ulva from freshwater ecosystems suggested that the density of Ulva thalli in mats was (fishpond, stream, water tank and river alluvium) in influenced by changes in sodium chloride and the Czech Republic. The author demonstrated that all phosphate concentrations. collected freshwater specimens of Ulva in the Czech 123 82 Aquat Ecol (2011) 45:75–87

Republic clearly belong to the species U. flexuosa,a seawaters (Ba¨ck et al. 2000; Blomster et al. 2000, well-known euryhalinic and common saltwater taxa. 2002). In the inland waters of Poland, large mats with Further research on the phylogeny of Ulva popula- surface areas up to 12 m2 formed by Ulva compressa tions present in freshwater ecosystems is necessary. and Ulva intestinalis have been found, among others, However, these works require the comparison of in Laskownickie Lake (Central Poland; Messyasz many holotypes from countries where new popula- 2009). The mats of Ulva in the studied streams were tions of these species may be identified in freshwater much smaller (up to 4 m2) and associated with the ecosystems. small streambed, shallow water and less water depth At present, there are over 50 sites identified as as factors influencing the size of the algal mats. M having these chlorophytes in Poland, and it is with the deepest water (89 cm) and the largest mats estimated that there are many more. However, it also had the greatest number of thalli. In the other has not been confirmed whether the species recorded two streams, the mats were small (DR) or appeared at these sites are still present. Well recognised and rarely and included only a few plants (S). A greater described sites have been reported by Plin´ski (1971, water depth at the analysed sites is associated not 1973a, b), who described Ulva species observed in only with a larger mat surface but also with higher Polish lakes. The fragmented knowledge of the inland thalli density of mats and thalli length. distribution of these species occurs, first, because Mats formed by Ulva species in a sea littoral zone there is a lack of sites where Ulva can survive and, may achieve a considerable biomass. In Finland, secondly, not recognising these macroalgae in fresh- coastal water mats of U. intestinalis covering an area water ecosystems. Few publications thoroughly dis- of 3.7 km2 have yielded a biomass of 32 tons since cuss the circumstances and reasons for the occurrence 1997 and 97 tons since 1993 (Ba¨ck et al. 2000). of Ulva in fresh waters (Plin´ski 1971, 1973a, b; U. intestinalis is currently a dominant Ulva species in Kowalski 1975; Sitkowska 1999). In most cases, most Scandinavian coastal waters and in Poland information about the occurrence of these chloro- (Haroon et al. 1999; Plin´ski and Jo´z´wiak 2004). In the phyte thalli in a given ecosystem has been restricted Polish , the number of U. compressa has lacking species identification and the site description decreased in favour of U. intestinalis (Plin´ski and during other limnological studies (Liebetanz 1925; Jo´z´wiak 2004). Bonsdorff et al. (1997) report multi- Piotrowska 1961;Da˛mbska 1976). Another important species mats are disappearing, whereas mono-spe- phenomenon is the occurrence of Ulva species in cies, e.g., U. intestinalis, is generally a very stable inland waters that are anthropogenically contami- population for a few years. In the freshwater ecosys- nated with sodium chloride (Messyasz 2009; Mess- tems studied here, Ulva populations also demon- yasz and Rybak 2009). Such contamination can reach strated continued annual development (personal small rivers and lakes in the form of rainwater runoff observation from 2004), and they grow to a size that flows mostly from city roads and motorways. similar to macroalgae patches. This type of contamination occurs in the three streams in this study. Thalli types

Macroalgae mats Freshwater forms of Ulva may have two types of thalli: (1) thalli characteristic of young plants that Massive blooms of various Ulva species in seawater have an intestinally undulating structure and (2) thalli are known to exist as free-floating individual plants or occurring in mature and senescing plants that have a as aggregations of thalli forming characteristic algal characteristic curly bubbled structure (Messyasz and mats (Leskinen et al. 2004; Pregnall 1983; Pregnall Rybak 2008a). The degree of mature thalli corruga- and Rudy 1985; Malta et al. 1999;Ba¨ck et al. 2000; tion may be connected with crystals of calcium Romano et al. 2003). The ability to form such carbonate, sulphates and chlorides covering the thal- aggregations seems to belong not only to individual lus. Scanning electron microscope observations of species but also to the whole Ulva genus. However, it Ulva thalli were carried out by us and that the surface is generally accepted that microalgal mats are more is covered with large numbers of diatoms, both in common in estuaries and contaminated coastal between and on the calcium carbonate crystals. Thus, 123 Aquat Ecol (2011) 45:75–87 83 the shape of thalli in young and mature plants results environmental factors, and the most important of not only from the ontogenetic cycle coded in the which are high concentrations of nutrients and genotype but is also influenced by other biotic and chlorides that stimulate thalli development (Plin´ski abiotic environmental factors. These factors signifi- 1971; Sitkowska 1999; Messyasz and Rybak 2008b). cantly affect the deformation of the thalli surface. The effect of the above-mentioned parameters on thalli structure, manifested by branching or lack of Competition branching, has been noticed in marine forms of U. compressa and U. intestinalis (Leskinen et al. Ulva mats are in serious competition for space with 2004). At low chloride concentrations, the thalli of other species including vascular plants (duckweed) both species were highly furcated. Moreover, and other filamentous algae (e.g. Cladophora and Leskinen et al. (2004) observed furcated thalli in Oedogonium) living in littoral waters. The domina- U. compressa and non-furcated thalli in U. intesti- tion of duckweed species at the studied sites occurred nalis on the coasts of Sweden, and after the macroalgae developmental optimum and . However, in areas with salinity higher during gradual senescence of the chlorophyte thalli. than 27 ppt non-furcated thalli of U. compressa and The prevalence of duckweed and Spirodela in the furcated thalli of U. intestinalis were present. Thus, surface water was possible not only due to a very it was concluded that the degree of thallus branching high reproduction rate of these species but also of U. intestinalis is connected with higher chloride because of a gradual slowing of the elongation concentrations more than for U. compressa. These growth and lack of young thalli development in Ulva. observations were confirmed in laboratory experi- Massive development of duckweed and Spirodela ments, where De Silva and Burrows (1973) proved species at the freshwater sites reduces the amount of that salinity significantly affects the branching light reaching algal thalli in deeper water. This stress ability of these species. The results of our studies leads to a change in colour of the thalli to dark green, suggest that the degree of branching of Ulva sp. resulting from increased concentrations of photosyn- thalli does not depend on sodium chloride concen- thetic pigments in the thallus cells. Such a colour tration but is slightly positively correlated with change of marine Ulva species’ thalli also depends on water temperature (r = 0.38; P \ 0.05). Whether the increasing water depth at which they grow. Thalli there is a stimulating effect of water temperature on sampled from deeper waters are darker than those thalli branching is unclear, and it is probable that the that grow closer to the surface. Moreover, De Valera degree of branching is also due to other, as of yet (1940) claims that this phenomena is caused by high unidentified, environmental factors. concentrations of nutrients in marine water, therefore Sites M1, M2, DR and S have received large loads the change in pigmentation can be used as a of chlorides, especially in winter, from the motorway contamination indicator. The last experimental ex since 2003. During periods of low temperatures, the situ examinations (Figueroa et al. 2009; Villares and motorway operator uses sodium chloride (in solution Carballeira 2004) conducted on marine species of and dry) and calcium chloride (only in solution) to Ulva (U. intestinalis, U. rigida, U. lactuca) also keep the road free from ice (personal communication, confirmed that nutrient availability has an influence Włodzimierz Matczak, assistant director of Motorway on the pigmentation of thalli and their photosyntheses Operations). It is likely that the motorway system of ratio. Han et al. (2008) point out that high concen- pre-treating water results in a regular dosage of trations of heavy metals (e.g. copper) also influence incoming chlorides to these streams. Comparative the pigmentation of Ulva thalli. At present, no similar studies of sodium chloride concentration carried out in information is available for Ulva thalli from fresh- summer, autumn and winter (taking into consideration water ecosystems. thawing and pre-thawing periods) showed constantly elevated levels of 528–613 mg L-1 (January 12, air Effects of chlorides and temperature temp. ?6°C) and 592–647 mg L-1 (December 15, air temp. -2°C). Heavy rains do not considerably affect The occurrence of Ulva species in freshwater chloride dilution in these streams. High sodium ecosystems in Poland is influenced by various chloride levels have a negative influence on the Ulva 123 84 Aquat Ecol (2011) 45:75–87 population, leading to reduced length and number of thalli (Villares and Carballeira 2004). The highest thalli and consequently decreasing the mat’s surface biomass growth rate of the chlorophytes occurred area. The decline in these morphometric parameters at phosphate concentrations of 20–30 mmol m-3 is visible at sodium chloride concentration [400 (Taylor et al. 2001). mg L-1. It was not determined what chloride con- Most studies regarding the ecology and distribu- centration in freshwaters leads to thalli development tion of marine Ulva species indicate that these algae or maintenance. This optimum level was impossible occur in areas with high concentrations of nitrogen to define, as throughout the whole observation period compounds, mostly of nitrate and ammonium. Fur- the level of sodium chloride was high for all mac- thermore, the appearance of large algal mats is a sign roalgae sites. Nevertheless, sodium chloride is one of of elevated levels of these compounds in the littoral the most important factors affecting the development regions of marine habitats (Sfriso et al. 1987; of Ulva in freshwater. Similarly, Messyasz (2009) Raffaelli et al. 1989; Fletcher 1992; 1996; Bonsdorff notes that low chloride concentrations in Laskownic- et al. 1997; Sfriso and Marconimi 1997; 1999; Sfriso kie Lake may be connected with faster thalli devel- et al. 2001; Martins et al. 2001). Our studies show opment in enriched waters. The distribution of Ulva that increasing concentrations of nitrates in freshwa- (e.g. U. compressa) in the Baltic Sea is, in turn, much ter lead to greater numbers of thalli in the microalgae more dependent on salinity than originally assumed mats of Ulva (r = 0.56; P \ 0.01), whereas the (Nielsen et al. 1995; Tolstoy and Wille´n 1997). In the influence of ammonium on the development of this work published by Leskinen et al. (2004) describing species is not statistically significant. the distribution of U. compressa along the Norwegian, Swedish, Finnish and Danish coasts, this species was not observed in waters with a salinity below 15 ppt. It Summary was then concluded that salinity is an important limiting factor of U. compressa distribution in the There is an important relationship between the Baltic Sea. These conclusions were confirmed in morphological features of Ulva and the salinity and experimental studies (Koemann and Van den Hoek nutrient concentrations in these freshwater habitats. 1982) that revealed that this alga does not grow in In addition, high concentrations of chlorides in the waters with low sodium chloride concentrations and water were unfavourable for development of the Ulva that only a minimal level is necessary for its proper thalli. Statistical analyses showed that the most development. Taylor et al. (2001) also report that essential physical factor positively correlated with U. compressa has a wide tolerance range towards salt development of Ulva mats was water depth. and grows in water of salinity ranging from 0 to 34 In order to better understand the ecology and psu. When there is a low concentration of chlorides, distribution of Ulva species in inland ecosystems, it the development of this species is restrained, and it is is necessary to intensify the studies at new freshwater the most effective at salinity of 6 to 8 psu. sites where these chlorophytes are located. It is probable that large macroalgal mats in freshwaters can have a considerable influence on both the water and Biogenic substances benthic organisms living under these mats, as shown for marine ecosystems. Therefore, it is necessary to Phosphates are another essential chemical parameter further examine reasons for the appearance of bloom- influencing the development of Ulva in freshwaters. forming mats of Ulva in freshwater ecosystems. Phosphorus concentrations are strongly positively correlated with thalli density of mats, the mat’s Acknowledgments We are grateful to Professor Lubomira surface area and average length of thalli forming the Burchardt for her helpful suggestions and critical comments on mat (r = 0.70; r = 0.52 and r = 0.59 for P \ 0.01, the manuscript. We also thank Dr. Maciej Ga˛bka for assisting respectively). This finding was confirmed in labora- in the statistical analyses. This research was financially tory studies that showed that P concentrations are supported by the Polish Ministry of Science and Higher Education (grant No. NN304 013437). We also thank the positively correlated with the photosynthesis rate of anonymous reviewers of this paper for the valuable, critical and U. compressa and consequently with the growth of its helpful comments on the manuscript. 123 Aquat Ecol (2011) 45:75–87 85

Open Access This article is distributed under the terms of the Fletcher RL (1992) The ‘‘green tide’’ problem. In: Schramm Creative Commons Attribution Noncommercial License which W, Nienhuis P (eds) Ecological studies, marine benthic permits any noncommercial use, distribution, and reproduction vegetation. EEC, Brussels, pp 29–33. doi: 10.1017/S0025 in any medium, provided the original author(s) and source are 315400034111 credited. Fletcher RL (1996) The occurrence of ‘‘green tide’’ problem. In: Schramm W, Nienhuis P (eds) Ecological studies, marine benthic vegetation. EEC, Brussels, pp 7–43. doi: 10.1017/S0025315400034111 Gabrielson PW, Widdowson TB, Lindstrom SC, Hawkes MJ, References Scagel RF (2000) Keys to the benthic marine algae and seagrasses of British Columbia, southeast Alaska, Wash- Ba¨ck S, Lehvo A, Blomster J (2000) Mass occurrence of ington and Oregon. Department of Botany, University of unattached Enteromorpha intestinalis on the Finnish British Columbia, Vancouver. doi: 10.1046/j.1529-8817. Baltic Sea coast. Ann Bot Fennici 37:155–161 2002.38101.x Bliding C (1963) A critical survey of european taxa in . Go¨ppert HR, Cohn F (1850) Ueber die Algen Schlesiens. U¨ bers Part 1. Casosiphonia, Blidingia, Enteromorpha. Opera Arbeiten Vera¨nd Schles Ges Vaterl Cultur 1:93–95 Bot 8(3):1–160 Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, Upper Bliding C (1968) A critical survey of european taxa in Ulvales. Saddle River, p 253 Part 2. Ulva, Ulvaria, Monostoma, Kornmannia. Bot Not Han T, Kang SH, Park JS, Lee HK, Brown MT (2008) Phys- 121:534–629 iological responses of Ulva pertusa and U. armoricana to Blomster J, Hoey EM, Maggs CA, Stanhope MJ (2000) Spe- copper exposure. Aquatic Toxicol 86:176–184. doi: cies-specific oligonucleotide probes for macroalgae: 10.1016/j.aquatox.2007.10.016 molecular discrimination of two marine fouling species of Haroon MA, Szaniawska A, Plin´ski M (1999) The distribu- Enteromorpha (Ulvophyceae). Mol Ecol 2:177–185. doi: tion, species compositions and abundance of Enteromor- 10.1046/j.1365-294x.2000.00850.x pha spp. in the Gulf of Gdan´sk. Oceanol Stud 28(1–2): Blomster J, Back S, Fewer DP, Kiirikki M, Lehvo A, Maggs 31–39 CA, Stanhope MJ (2002) Novel morphology in Entero- Hayden HS, Blomster J, Maggs CH, Silva P, Stanhope M, morpha (Ulvophycae) forming green tides. Amer J Bot Waaland R (2003) Linnaeus was right all along: Ulva and 89:1756–1763. doi:10.3732/ajb.89.11.1756 Enteromorpha are not distinct genera. Eur J Phycol Bonsdorff E, Blomqvist EM, Mattila J, Norkko A (1997) 38:277–294. doi:10.1080/1364253031000136321 Coastal eutrophication: cause, consequences and per- Ichihara K, Arai S, Uchimura M, Fay EJ, Ebata H, Hiraoka M, spectives in the archipelago areas of the northern Baltic Shimada S (2009) New species of freshwater Ulva, Ulva Sea. Estuar Coast Shelf Sci 44:63–72. doi:10.1016/S02 limnetica (Ulvales, Ulvophyceae) from the Ryukyu 72-7714(97)80008-X Islands, Japan. Phycol Res 57:94–103. doi:10.1111/j. Callow ME, Callow JA, Pickett Heaps JD, Wetherbee R (1997) 1440-1835.2009.00525.x Primary adhesion of Enteromorpha (Chlorophyta, Ulva- Kirchhoff A, Pflugmacher S (2002) Comparison of the detox- les) propagules: quantitative settlement studies and video ication capacity of limnic and marine form of the green microscopy. J Phycol 33:938–947 algae Enteromorpha compressa. Marine Envirn Res Da˛mbska I (1976) Materials of the study of peryphiton of the 50:60–81. doi:10.1016/S0141-1136(00)00251-8 Konin Lakes. Seria Biol Uniw A Mickiewicz in Poznan´ Koemann R, Van den Hoek C (1982) The of 6:85–90 Enteromorpha link, 1820 (Chlorophyceae) in The De Silva MW, Burrows EM (1973) An experimental assess- Netherlands. I. The section Enteromorpha. Arch Hydro- ment of the status of the species Enteromorpha intestinalis biol Suppl 63:279–330 (L.) Link and Enteromorpha compressa (L.) Grev. Kowalski W (1975) Occurrence of the species of a Marine J Marine Biol Assoc UK 53:895–904. doi: 10.1017/S002 Green Alga Enteromorpha Link (1982) in the Szczecin 5315400022554 Pomerania inland waters. Fragm Flor Geobot Ser Polonica De Valera M (1940) Note on the difference in growth of 21:527–536 Enteromorpha species in various culture media. Kgl Kozłowski W (1890) Introduction to the flora from the Fysiogr Sallsk Lund Forhandl 10(5):52–58 vicinity of the Ciechocinek. Pam Fizjogr 10:1–3 Endler Z, Goz´dziejewska A, Jaworska B, Grzybowski M Lee RE (1999) Phycology, III. Cambrige University Press, (2006) Impact of small hydropower station on Plankton Cambrige, p 614 organisms in river water. Acta Sci Pol Formatio Circu- Leghari SM, Jafri SIH, Mahr MA, Lashari KH, Ali SS, miectus 5(2):121–134 Jahangir TM, Khuahawar MY (2000) Limnological Study Figueroa FL, A, Neori A, Martinez B, Malta EJ, Put Ang of Sonharo, Mehro Pateji and Cholari Lakes of District J, Inken S, Marquardt R, Korbee N (2009) Effects of Badin, Sindh Pakistan. Pakistan J Biol Sci 3(11):1904– nutrient supply on photosynthesis and pigmentation in 1909 Ulva lactuca (Chlorophyta): responses to short-term Leskinen E, Alstro¨m-Rapaport C, Pamilo P (2004) Phytogeo- stress. Aquat Biol 7:173–183. doi:10.3354/ab00187 graphical structure, distribution and genetic variation of Fish JD, Fish S (1989) A student’s guide to seashore. Uniwin the Ulva intestinalis and U. compressa Hyman Ltd. London 11:35–36. doi:10.1017/S00253154 (Chlorophyta) in the Baltic Sea area. Mol Ecol 13: 00034391 2257–2265. doi:10.1111/j.1365-294X.2004.02219.x 123 86 Aquat Ecol (2011) 45:75–87

Liebetanz B (1925) Hydrobiologische Studien an Kujawischen the Gulf of Gdan´sk in 1979 and 1980. Oceanologia 19: Brackwa¨ssern. Bull Intern Acad Polon Sci Lettres Sci 101–115 Math Nat Ser B Sci Mat, pp 116 Plin´ski M, Jo´z´wiak T (2004) The distribution of water vege- Malta EJ, Draisma SGA, Kamermans P (1999) Free floating tation on the Polish coast of the Baltic sea in 1996–2000. Ulva in the southwest Netherlands: species or morpho- Oceanol Hydrobiol Stud 32(2):29–40 types? A morphological, molecular and ecological com- Plin´ski M, Manasterska M, Florczyk I (1982) The preliminary parison. Eur J Phycol 34:443–454. doi:10.1080/095414 ecological characteristic of genus Enteromorpha (Link) in 49910001718801 the Bay of Gdan´sk. Zesz Nauk. Wydz. Biol. Nauk Ziemi, Marczek E (1954) A New locality of Enteromorpha intestinalis Oceanografia, Uniw Gdan´sk 9(1):65–80 (L.) Link Ku¨tzig [(L.) Greville] and Enteromorpha tu- Pregnall AM (1983) Release of dissolved organic carbon from bulosa J. G. Agardh. Fragm Flor Geobot Ser Polonica 2: the estuarine intertidal macroalga Enteromorpha prolif- 105–111 era. Mar Biol 73:37–42. doi:10.1007/BF00396283 Maresˇ J (2009) Combined morphological and molecular Pregnall AM, Rudy PP (1985) Contribution of green macro- approach to the assessment of Ulva (Chlorophyta, Ulvo- algal mats (Enteromorpha ssp.) to seasonal production in phyceae) in the Czech Republic. Master thesis. University an estuary. Mar Ecol Prog Ser 24:167–176 of South Bohemia, Faculty of Science, Department of Raciborski M (1910) Phycotheca polonica. Part 1, Kosmos. Botany 35:80–89, 1001–1006 Martins I, Pardal MA, Lillebo AI, Flindt MR, Marques JC Raffaelli D, Hull S, Milne H (1989) Long-term changes in (2001) Hydrodynamics as a major factor controlling the nutrients, weed mats and shorebirds in an estuarine sys- occurrence of green macroalgal blooms in a eutrophic tem. Cah Biol Mar 30:259–270 estuary: a case study on the influence of precipitation and Reinke DC (1981) Enteromorpha, a Marine Alga in Kansas. river management. Estuar Coast Shelf Sci 52:165–177. Trans Kansas Academy Sci 84(4):228–230. doi:10.2307/ doi:10.1006/ecss.2000.0708 3628281 McAvoy KM, Klug JL (2005) Positive and negative effects of Romano C, Windows J, Brinsley MD, Staff FJ (2003) Impact riverine input on the estuarine green alga U. intestinalis of Enteromorpha intestinalis mats on near-bed currents (syn. E. intestinalis) (Linneus). Hydrobiologia 545:1–9. and sediment dynamics: flume studies. Mar Ecol Prog Ser doi:10.1007/s10750-005-1923-5 256:63–74. doi:10.3354/meps256063 Messyasz B (2009) Enteromorpha (Chlorophyta) populations Sfriso A, Marconimi A (1997) Macrophyte production in a in River Nielba and Lake Laskownickie. Oceanol shallow coastal lagoon. Part I. Coupling with chemico- Hydrobiol Stud 38(1):1–9 physical parameters and nutrient concentrations in waters. Messyasz B, Rybak A (2008a) New inland localities of salt- Mar Environ Res 44:351–375. doi:10.1016/S0141-113 like green alga Enteromorpha compressa (L.) Ness in 6(97)00012-3 Poland. Badania Fizjograficzne nad Polska˛ Zachodnia˛, Sfriso A, Marconimi A (1999) Macrophyte production in a Seria B—Botanika 57:77–88 shallow coastal lagoon. Part II. Coupling with sediment, Messyasz B, Rybak A (2008b) Occurrence of Enteromorpha SPM and tissue carbon, nitrogen and phosphorus con- compressa [syn. Ulva compressa (L.)] (Chlorophyta) in centrations. Mar Environ Res 47:285–309. doi:10.1016/ the Wielkopolska Region. Fragm Flor Geobot. Ser Polo- S0141-1136(98)00122-6 nica 15(1):17–19 Sfriso A, Marcomini A, Pavoni B (1987) Relationships Messyasz B, Rybak A (2009) The distribution of green algae between macroalgae biomass and nutrient concentrations species from the Ulva genera [syn. Enteromorpha; Chlo- in the hypertrophic area of the Venice lagoon. Mar Env rophyta] in Polish inland waters. Oceanol Hydrobiol Stud Res 22:297–312. doi:10.1016/0141-1136(87)90005-5 38(1):121–138. doi: 10.2478/v10009-009-0001-0 Sfriso A, Birkemeyer T, Ghetti PF (2001) Benthic macrofauna Namysłowski B (1927) Hydrobiology research. Prace Komis changes in areas of Venice lagoon populated by seag- Mat Przyrod Poz Tow Przyj Nauk Ser B Nauk Biolog rasses or . Mar Environ Res 52:323–349. doi: 1:1–13 10.1016/S0141-1136(01)00089-7 Nielsen R, Kristiansen A, Mathiesen L, Mathiesen H (1995) Sitkowska M (1999) Two new localities from Enteromorpha Distributional index of the benthic macroalgae of the flexuosa subsp. pilifera (Chlorophyta) in Poland. Fragm Baltic Sea area. Acta Botanica Fennica 155:1–51 Flor Geobot Ser Polonica 6:301–304 Piotrowska H (1961) Halophytes near the Kołobrzeg. Chron´my Starmach K (1972) Green alga. In: Starmach K (ed) Freshwater Przyr Ojcz 17(4):24–28 flora of Poland. PWN, Warszawa-Krako´w, p 163 Plin´ski M (1971) The species of Enteromorpha (Link) Agardh Taft CE (1964) The occurrence of Monostoma and Entero- genus from the area of salt pans near Łe˛czyca. Zesz Nauk morpha in Ohio. Ohio J Sci 64(4):272–273 UŁ Biol 41:159–169 Taylor R, Fletcher RL, Raven JA (2001) Preliminary studies on Plin´ski M (1973a) The algae of salt marshes near Łe˛czyca, the growth of selected ‘‘green tide’’ algae in laboratory Central Poland. Monogr Bot 39:3–88 culture: effects of irradiance, temperature, salinity and Plin´ski M (1973b) A new locality of Enteromorpha intestinalis nutrients on growth rate. Bot Mar 44:327–336. doi: (L.) Greville in Poland. Fragm Flor Geobot Ser Polonica 10.1515/BOT.2001.042 19(1):135–137 Tolstoy A, Wille´n T (1997) Preliminary checklist of macro- Plin´ski M, Florczyk I (1984) Analysis of the composition and algae in Sweden. Artdatabanken. Agricultural University vertical distribution of the macroalgae in Western part of of Sweden, Uppsala, pp 6–10

123 Aquat Ecol (2011) 45:75–87 87

Torka V (1910) Zur Erforschung Posener Algen. Zeitschr d Wilkon´-Michalska J (1963) The halophytes from Kujawy. Stud Naturw Abt 16:179–187 Soc Sc Tor Sect D 7(1):1–121 Villares R, Carballeira A (2004) Nutrient limitation in Mac- Williams CH (1993) Processes of Aquatic Weed Invasions: the roalgae (Ulva and Enteromorpha) from the Rias Baixas New Zealand example. J Aquat Plant Manage 31:17–23 (NW Spain). Mar Ecol 25(3):225–243. doi:10.1111/j. Wysocka H (1952) The Marine alga in the Wisła River near 1439-0485.2004.00027.x Warsaw. Gazeta Obserwatora PIHM 5(4):7–10 Wallentinus I (1979) Environmental influences on benthic Zbikowski_ R, Szafer P, Latała A (2005) Distribution and macrovegetation in the Trosa-Asko¨ area, northern Baltic relationships between selected chemical elements in green proper. II. The ecology of macroalgae and submersed alga Enteromorpha sp. from the southern Baltic. Envir phanerogams. Contributions to the Asko¨ Laboratory. Poll 3:435–448. doi:10.1016/j.envpol.2005.12.007 University of Stockholm, pp 1–210 Whitton BA, Dalpra M (1968) Floristic changes in the River Tees. Hydrobiologia 32:545–550. doi:10.1007/BF0015 5407

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